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Evolution in Structured Populations

The phenotype as the center of Evolution

When I first learned about evolution I was taught that evolution was change in gene frequency. As I pointed out before this definition is inadequate, however, the gene frequency definition has the interesting property that evolution can be described in terms of deviations from the Hardy-Weinberg-Castle (HWC) equilibrium. For all its faults the HWC equilibrium gives us a familiar starting place for discussing the forces of evolution.

Consider a one-locus two-allele system with an A1 and an A2 allele. If the frequency of the A1 allele is p, and the frequency of the A2 allele is q (p + q = 1), then the HWC proportions are simply given by (p + q)2:

A1A1

A1A2

A2A2

p2

2pq

q2

This result was independently “discovered” by Hardy, Weinberg, and Castle, which is why it bears their name. (Note I put discovered in quotes. Hardy, at least, was always a bit embarrassed that his name was attached to such an obvious result, and Castle’s graduate student, Sewall Wright, is reputed, although I can’t find a reference to this, to have referred to it as the “well known law of proportions”).

Importantly, the HWC equilibrium (as opposed to the proportions) is a phenomenon in which the HWC proportions are maintained for multiple generations, and gene frequencies and genotype frequencies do not change. This was the beauty of the “change in gene frequencies” definition of evolution. The HWC equilibrium forms a null hypothesis for that definition: If the HWC equilibrium holds then evolution is not occurring.

To move towards a phenotypic view of evolution we need to think about the informational function of genes. As I described in my last post, genes are a bit complex in that they have three different functions. They transmit information between generations, they interact with other genes and other heritable elements and the environment to create the phenotype, and they (or at least their sequence and position in the genome) are part of the phenotype. It is the transmission of information between generations aspect of genes that is of interest here.

Think of the birth of a new individual to be the creation of a new phenotype based on standard rules. In our simple one locus two allele genetic system the rules are that the offspring’s phenotype is determined by randomly selecting one allele from each parent. It is convenient to think of the phenotype of the offspring to be determined by a “transition equation” that converts the phenotypes of the parents into the phenotype of the offspring.

In our simple genetic system the simplest phenotype is the number of A1 alleles. Thus, an A1A1 individual has a phenotype of 2, an A1A2 a phenotype of 1, and an A2A2 a phenotype of 0. From this we can easily set up a table of the possible phenotypes that any pair of parents can produce:

Father’sPhenotype (andgenotype)

Mother’s phenotype (and genotype)

2 (A1A1)

1 (A1A2)

0 (A2A2)

2 (A1A1)

2 (A1A1)

1.5 (A1A1 & A1A2)

1 (A1A2)

1 (A1A2)

1.5 (A1A1 & A1A2)

1 (A1A1 & A1A2 &A2A2)

0.5 (A2A2& A1A2)

0 (A2A2)

1 (A1A2)

0.5 (A2A2& A1A2)

0 (A2A2)

Thus, in this simple world the transition equation translating the phenotypes of the parents into the mean phenotype of the offspring is clear, and easily described as the mean of the two parents. Note that even here, however, there is a stochastic element. We can predict the mean phenotype for the offspring, but not its actual value. For example in a cross between two A1A2 individuals, the mean phenotype of the offspring is one, but it is impossible to exactly predict the phenotype of a specific offspring from the parental phenotypes.

In real systems with gene interaction, maternal effects, epigenetics, culture etc. the transition equations governing the formation of phenotypes are far more complicated, and almost certainly contain both discrete (genes) and continuous (culture) elements. Although it may be computationally difficult, there is no conceptual difficulty in adding additional factors to the “transition equation” from parental phenotypes to offspring phenotypes. In essence the transition equation of phenotypes in one generation to phenotypes in the next is simply the rules of inheritance for the factors that contribute to the patterning node described in the previous post.

Nothing is lost and much is gained viewing these Mendelian rules as “transition equations” that convert phenotypes one generation into phenotypes in the next generation. For example, one of the serious problems with the gene centric view of evolution is how to incorporate cultural inheritance. Culture is inherently a continuous phenomenon. You learn language primarily from your parents, but also from many others. I grew up in the Midwest, but my children grew up in Vermont. They swallow their t’s just like any red blooded Vermon’er does, and they did not learn that from me. Language is certainly heritable, but the rules are not discrete or simple like the Mendelian rules I outlined above. Incorporating continuous factors such as culture, and the complications of multiple cultural “parents” is a technical difficulty, but not a conceptual difficulty for the phenotypic view of evolution.

Note the strong contrast of this phenotypic view to the Dawkinsian genic view of evolution. In the phenotypic view of the world “genes” take on the subservient role of simply being mathematical constructs (transition equations) that have a physical reality in the form of DNA. In the genic view genes are central in evolution. In this view the genes are immortal “replicators” and create “vehicles” (phenotypes) that carry them forward to the next generation. You can’t make this stuff up. Here is the real quote: “The fundamental units of natural selection, the basic things that survive or fail to survive, that form lineages of identical copies with occasional random mutations, are called replicators. DNA molecules are replicators. They generally, . . ., gang together into large communal survival machines or ‘vehicles’. The vehicles that we know best are individual bodies like our own.” (Dawkins, The Selfish Gene). From a phenotypic perspective this quote is just silly.

I think Dawkin’s concept of the “meme” is particularly telling. As I pointed out culture is intrinsically continuous and no problem for the phenotypic view of evolution; however, for the genic view it is a huge problem. In Dawkin’s view the gene as an object is the center of evolution. Culturally inherited traits cannot be objects from the genic perspective unless they are atomized. The meme is an attempt to force this intrinsically continuous concept into the particulate framework that is essential for the genic view of evolution.

Historically I find this fascinating, since in the early 1900’s the Biometricians refused to accept the idea of particulate inheritance. Fisher came along and saved us by explaining how particles of infinitesimal effect could appear continuous. From that we became so enamored of genes and particulate inheritance that when our theory eventually was confronted with an aspect of inheritance that was continuous we find Dawkins being the mirror image of the biometricians and refusing to accept continuous inheritance.

If I may be a bit sarcastic for a moment (and I have always wanted to do this), to paraphrase Wolfgang Pauli, Dawkins isn’t right, he’s not even wrong. The only “replicator” I am aware of was invented by Xerox, and in the living world the only “vehicles” I am aware of are horses, but only when they are wearing saddles. (My colleagues point out that we need to include donkeys, camels and especially elephants – can’t forget elephants – in our definition of vehicles.)

7 Responses to “The phenotype as the center of Evolution”

“However, now when somebody says “gene” I have to ask, do they mean the ORF, the exon, the intron, the promoter? From a phenotypic perspective we actually can define gene: it is a unit that is inherited with sufficient fidelity that we can consider it to be a particle. What that object actually is may vary depending on the circumstances. We also are not upset when the object gets changed as a result of a crossover event breaking it up or a transposon inserting in the middle of it. This just becomes a “mutation”.”

The definition of a gene can vary, I agree. But this is by no means inconsistent with a gene centric view. I would define a gene as a region of DNA that contributes to a phenotype–it is also heritable. The phenotype is then subject to selection. My definition includes regulatory elements(promoters, cis-regulatory elements, introns, 5′ UTR, 3′ UTR), protein coding exons, and even RNA(tRNA, microRNAs, long non-coding RNAs etc). Mutations are not a problem for a gene centric view.

These comments are getting too long. I will not respond point by point, and perhaps I should do it as a new post. On a few of the points: Yes, I am saying that genes are not discrete. The nice concept of the “gene” as a bead on a string was a reasonable approximation in the 1970’s when Dawkins wrote the selfish gene. However, now when somebody says “gene” I have to ask, do they mean the ORF, the exon, the intron, the promoter? From a phenotypic perspective we actually can define gene: it is a unit that is inherited with sufficient fidelity that we can consider it to be a particle. What that object actually is may vary depending on the circumstances. We also are not upset when the object gets changed as a result of a crossover event breaking it up or a transposon inserting in the middle of it. This just becomes a “mutation”.

I do think that memes are relevant here. It is very telling that Dawkins had to invent memes, and the acquisition of language is a good model for this. Memes do not exist, end of story. What does exist is a language, and the process by which infants acquire language. That is not a set of memes that is acquired, it is simply a process of copying and learning from other people. It is tempting to point to things like letters as being discrete “meme like” entities, but written language is a derived skill that comes about somewhat later in life. It is something that we have developed a set of rules (traditions, I am not sure what to call them) that allow us to communicate. Yes, our alphabet has been reified into 26 distinct symbols, but even those are subject to change. On the one hand there are a number of symbol pairs that really are distinct letters (fi, ch, kn), there are hundreds of fonts, and an infinite number of ways to hand write letters. Until the advent of the modern dictionary it was considered to be a mark of being a dullard if you always spelled things the same way (can you say leftenant?). Even an cultural item as distinct as letters is malleable, learned from others without the help of a “meme”.

If Dawkins does believe genes have a purpose, I would disagree. I think a gene centric view of evolution is a process with no purpose.

“The reason Dawkins can call genes replicators is that according to him they copy themselves exactly, and are fixed objects that persist through evolutionary time.”

Well, he acknowledges that genes aren’t completely fixed and that there is variation within a gene, hence alleles.

“As such, in his view, selection acts on the individual genes and eventually leads them to clothe themselves in phenotypes to carry them forward.”

I disagree, I interpret his book as, selection acts directly upon the phenotype, and has fitness consequences for the genes because they cause phenotypes.

“More importantly, because of gene interactions what a gene does to the phenotype is very haphazard, and the relationship between a specific allele and fitness is, generally speaking, very tenuous.”

I disagree. Take a panel of embryo lethal genes as an example. Deleterious mutations in these genes that lead to loss of function(as an example) will have strong negative fitness consequences. This shows the importance of genes and strong influence on phenotypes.

“This is highlighted in the case of culture and Dawkins’ “memes”. Consider language. The concept of “mother tongue” is real. This is the language we learn as infants. It is nearly a certainty that your mother tongue will be the language of your primary care giver (in most cases your parents). Thus, it is clearly heritable, and just as clearly not genetic. What is interesting, however, is you do not learn your parent’s language exactly. You learn a language that is fully understandable to them, but has changes picked up from other “cultural parents” and peers. Thus, it is not the immutable object that persists through time. Just as importantly, the language you speak IS the trait, not the vehicle that carries the meme. There is no meme, only the acquisition of language from other individuals.”

How are you disputing memes? The components of language are discrete-letters, words are discrete. Ideas can be discrete and can be tracked/traced. Genes and memes are not exactly alike, Dawkins notes this. We can see that memes have greater horizontal transmission.

“This is the problem that Dawkins has. He is forcing himself into a box where genes are discrete entities. It is clear that language and culture simply does not fit in that box, and to get it in there, Dawkins has to go through unreasonable and frankly laughable logical contortions. But, consider genes: They are presumable strips of DNA, but are they really discrete entities? Many genetic diseases (e.g. Huntington’s Disease) are examples of slippage mutations on tandem repeats. These also don’t fit into Dawkin’s gene as discrete object.”

Genes are discrete entities, are you saying they’re not? And you’re jumping from genes are discrete to flaws in memes. Dawkin’s formulation of memes does not perfectly resemble genes, but the notes they are ‘replicators’.
Anyway, huntington’s disease is completely compatible with a gene centric view of evolution. Variants of the huntingtin gene cause the disease.
And methylation of a gene is an extension of gene-gene interactions. Most likely, a set of gene-gene interactions determines the methylation status–which can be attributed to variation of genes in this network. Consistent with a gene-centric view of evolution.

“My final point is that Dawkins terms DNA “immortal coils”, as if genes in some sense transcended time, and he views the soma as disposable and of little interest in evolution other than carrying genes forward. The problem is that we see huge amounts of variation in genomes over time. Sex chromosomes appear to have evolved multiple times, genes move around the genome, chromosomes fuse and fission. The bottom line is that phenotypic aspects of Dawkins’ immortal coils are not qualitatively different than any other aspect of the phenotype of an organism. They can and do change through time. There is no reason to privilege them over any other aspect of the phenotype. The only real difference between DNA, and say the width of your nose, is that genes act to transfer information between generations. However, so do mitochondria, and culture, and vertically transmitted bacteria. Genes are not special.”

This is not an argument against a gene centric view of evolution. As I pointed out earlier, a gene centric view does not exclude variation of genes or their positions. Its compatible. Replicators replicate, but they’re not perfect and processes such as mutations, recombination, genomic duplications leads to variation. Processes leading to these genomic variation exist because they survived. Dawkins also notes that genes ‘work’ together to survive better(fitness). The downstream effects of genes ‘working’ or interacting together leads to various levels of phenotypes.

“From my understanding and interpretation of the Selfish Gene, Dawkins uses shortcuts in his language . . . it is easier to write as if genes do have a purpose.”

I won’t argue with you on this one. Suffice it to say we disagree.

“Sorry, I am having trouble understanding this argument. Why are ‘genes as replicators’ silly?”
The reason Dawkins can call genes replicators is that according to him they copy themselves exactly, and are fixed objects that persist through evolutionary time. As such, in his view, selection acts on the individual genes and eventually leads them to clothe themselves in phenotypes to carry them forward. There are lots of problems with this. First, genes are not the constants he wishes they were. More importantly, because of gene interactions what a gene does to the phenotype is very haphazard, and the relationship between a specific allele and fitness is, generally speaking, very tenuous. This is highlighted in the case of culture and Dawkins’ “memes”. Consider language. The concept of “mother tongue” is real. This is the language we learn as infants. It is nearly a certainty that your mother tongue will be the language of your primary care giver (in most cases your parents). Thus, it is clearly heritable, and just as clearly not genetic. What is interesting, however, is you do not learn your parent’s language exactly. You learn a language that is fully understandable to them, but has changes picked up from other “cultural parents” and peers. Thus, it is not the immutable object that persists through time. Just as importantly, the language you speak IS the trait, not the vehicle that carries the meme. There is no meme, only the acquisition of language from other individuals.

This is the problem that Dawkins has. He is forcing himself into a box where genes are discrete entities. It is clear that language and culture simply does not fit in that box, and to get it in there, Dawkins has to go through unreasonable and frankly laughable logical contortions. But, consider genes: They are presumable strips of DNA, but are they really discrete entities? Many genetic diseases (e.g. Huntington’s Disease) are examples of slippage mutations on tandem repeats. These also don’t fit into Dawkin’s gene as discrete object. Other genetic diseases (Angelman’s syndrome and Prader-Willi syndrome) are affected by which parent they come from, and thus presumably by methylation state or other non-genetic modifications. These also don’t fit into Dawkin’s view of gene as object. One does not expect a model to have all the answers, but a good model can be conceptually extended to include complications. Dawkin’s gene centric view is sophomoric, and based on a string of beads model of genes. The world is not like that and that is a big problem with his view.

My final point is that Dawkins terms DNA “immortal coils”, as if genes in some sense transcended time, and he views the soma as disposable and of little interest in evolution other than carrying genes forward. The problem is that we see huge amounts of variation in genomes over time. Sex chromosomes appear to have evolved multiple times, genes move around the genome, chromosomes fuse and fission. The bottom line is that phenotypic aspects of Dawkins’ immortal coils are not qualitatively different than any other aspect of the phenotype of an organism. They can and do change through time. There is no reason to privilege them over any other aspect of the phenotype. The only real difference between DNA, and say the width of your nose, is that genes act to transfer information between generations. However, so do mitochondria, and culture, and vertically transmitted bacteria. Genes are not special.

“I am philosophically bothered by Dawkins implication that genes have a purpose, which is to survive and make copies of themselves. ”

From my understanding and interpretation of the Selfish Gene, Dawkins uses shortcuts in his language. He doesn’t really believe or advocate that genes have a purpose or have wants and desires. To me, he is writing more poetically or metaphorically and it is easier to write as if genes do have a purpose.

“I also think the silliness of the genes as replicators becomes obvious when we start thinking about continuous traits…”

Sorry, I am having trouble understanding this argument. Why are “genes as replicators” silly?

“Dr. Goodnight, I don’t see how describing an organism as a vehicle is silly. Can you elaborate please?”

One of Dawkins’ central ideas is that genes are immortal objects that create ephemeral phenotypes to carry them forward to the next generation. I specifically said that it was silly from a phenotypic perspective because this perspective turns the world upside down compared to Dawkins. Far from phenotypes being manipulated by the controlling genes, from the phenotypic perspective genes are parts of transition equations that are, if anything, manipulated by phenotypes.

I actually don’t accept either of those statements since both imply that one is controlling the other. This to me is the larger philosophical problem with Dawkins. Interestingly his book implies that genes have goals (e.g., to beat other genes and copy themselves). It is important to remember that nothing has a purpose or goals in an evolutionary sense. An organism either does or doesn’t reproduce. It may have evolved a desire for sex, but this is evolved because organisms who desire sex leave more offspring. I am philosophically bothered by Dawkins implication that genes have a purpose, which is to survive and make copies of themselves.

I also think the silliness of the genes as replicators becomes obvious when we start thinking about continuous traits, which is why I dwell on these so much. I don’t want to pretend that genes and particulate inheritance are not important, and in all likelihood for most organisms THE important mode of inheritance. It is just that if we want to take apart an issue the place to look is where the seams are unraveling.

“You also state that culture is “intrinsically continuous”, but there are cases where ‘subunits’ of culture such as ideas can be discrete, do you agree? For example, ideas can be tracked through hashtags on twitter/facebook.”

In polygenic systems particulate inheritance looks very much like it is a continuous trait. Thus, we find that with Mendelian genetics we have variation that looks continuous. I would argue that the opposite is also true. Often “memes” float around the internet; but are they really particles of culture, or are they cultural elements that are continuous, but appear to be particulate. I actually think there is some important confusion surrounding cultural evolution, but I have not sorted it out for myself just yet, and I am not really ready to talk about it.

Dr. Goodnight, I don’t see how describing an organism as a vehicle is silly. Can you elaborate please?

You also state that culture is “intrinsically continuous”, but there are cases where ‘subunits’ of culture such as ideas can be discrete, do you agree? For example, ideas can be tracked through hashtags on twitter/facebook.